PCaP2 regulates nuclear positioning in growing Arabidopsis thaliana root hairs by modulating filamentous actin organization

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• 作者：Yan Zhang ; Erfang Kang ; Ming Yuan ; Ying Fu ; Lei Zhu
• 关键词：Nucleus ; Root hair ; Tip growth ; Actin filament ; Actin ; binding protein ; Arabidopsis thaliana
• 刊名：Plant Cell Reports
• 出版年：2015
• 出版时间：August 2015
• 年：2015
• 卷：34
• 期：8
• 页码：1317-1330
• 全文大小：3,906 KB
• 参考文献：Balu拧ka F, Salaj J, Mathur J, Braun M, Jasper F, 艩amaj J, Chua N, Barlow PW, Dieter Volkmann D (2000) Root hair formation: f-actin-dependent tip growth is initiated by local assembly of profilin-supported F-Actin meshworks accumulated within expansin-enriched bulges. Dev Biol 227:618鈥?32PubMed View Article
  Bibikova T, Blancaflor E, Gilroy S (1999) Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana. Plant J 17:657鈥?65PubMed View Article
  Bloom K (2001) Nuclear migration: cortical anchors for cytoplasmic dynein. Curr Biol 11:326鈥?29View Article
  Carol RJ, Dolan L (2002) Building a hair: tip growth in Arabidopsis thaliana root hairs. Phil Trans R Soc Lond B 357:815鈥?21View Article
  Chen CY, Wong EI, Vidali L, Estavillo A, Hepler PK, Wu HM, Cheung AY (2002) The regulation of actin organization by actin-depolymerizing factor in elongating pollen tubes. Plant Cell 14:2175鈥?190PubMed Central PubMed View Article
  Chen P, Gao R, Chen S, Pu L, Li P, Huang Y, Lu L (2012) A pericentrin-related protein homolog in Aspergillus nidulans plays important roles in nuclear positioning and cell polarity by affecting microtubule organization. Eukaryot Cell 11:1520鈥?530PubMed Central PubMed View Article
  Cheung AY, Duan QH, Costa SS, de Graaf BH, Di Stilio VS, Feijo J, Wu HM (2008) The dynamic pollen tube cytoskeleton: live cell studies using actin-binding and microtubule binding reporter proteins. Mol Plant 1:686鈥?02PubMed View Article
  Chytilova E, Macas J, Sliwinska E, Rafelski SM, Lambert GM, Galbraith DW (2000) Nuclear dynamics in Arabidopsis thaliana. Mol Biol Cell 11:2733鈥?741PubMed Central PubMed View Article
  Cole RA, Fowler JE (2006) Polarized growth: maintaining focus on the tip. Curr Opin Plant Biol 9:579鈥?88PubMed View Article
  Diet A, Link B, Seifert GJ, Schellenberg B, Wagner U, Pauly M, Reiter W, Ringlia C (2006) The Arabidopsis root hair cell wall formation mutant lrx1 is suppressed by mutations in the RHM1 gene encoding a UDP-l -rhamnose synthase. Plant Cell 18:1630鈥?631PubMed Central PubMed View Article
  Dolan L, Duckett CM, Grierson C, Linstead P, Schneider K, Lawson E, Dean C, Poethig S, Roberts K (1994) Clonal relationships and cell patterning in the root epidermis of Arabidopsis. Development 120:2465鈥?474
  Fan JL, Wei XZ, Wan LC, Zhang LY, Zhao XQ, Liu WD, Hao HQ, Zhang HY (2011) Disarrangement of actin filaments and Ca2+ gradient by CdCl2 alters cell wall construction in Arabidopsis thaliana root hairs by inhibiting vesicular trafficking. J Plant Physiol 168:1157鈥?167PubMed View Article
  Iwabuchi K, Minamino R, Takagi S (2010) Actin reorganization underlies phototropin-dependent positioning of nuclei in arabidopsis leaf cells. Plant Physiol 152:1309鈥?319PubMed Central PubMed View Article
  Jones M, Nicholas Smirnoff N (2006) Nuclear dynamics during the simultaneous and sustained tip growth of multiple root hairs arising from a single root epidermal cell. J Exper Bot 57:4269鈥?275View Article
  Kato M, Nagasaki-Takeuchi N, Ide Y, Tomioka R, Maeshima M (2010) PCaPs, possible regulators of PtdInsP signals on plasma membrane. Plant Signal Behav 5:848鈥?50PubMed Central PubMed View Article
  Kato M, Aoyama T, Maeshima M (2013) The Ca2+-binding protein PCaP2 located on the plasma membrane is involved in root hair development as a possible signal transducer. Plant J 74:690鈥?00PubMed View Article
  Ketelaar T, Emons AMC (2001) The cytoskeleton in plant cell growth: lessons from root hairs. New Phytol 152:409鈥?18View Article
  Ketelaar T, Emons AMC (2009) The actin cytoskeleton in root hairs: a cell elongation device. In: Emons AMC, Ketelaar T (eds) root hairs. Springer-Verlag, Berlin Heidelberg, pp 211鈥?32View Article
  Ketelaar T, Faivre-Moskalenko C, Esseling JJ, de Ruijter NCA, Grierson CS, Dogterom M, Emons AMC (2002) Positioning of nuclei in Arabidopsis root hairs: an actin-regulated process of tip growth. Plant Cell 14:2941鈥?955PubMed Central PubMed View Article
  Ketelaar T, de Ruijter NCA, Emons AMC (2003) Unstable F-actin specifies the area and microtubule direction of cell expansion in Arabidopsis root hairs. Plant Cell 15:285鈥?92PubMed Central PubMed View Article
  Lee YJ, Yang ZB (2008) Tip growth: signaling in the apical dome. Curr Opin Plant Biol 11:662鈥?71PubMed Central PubMed View Article
  Libault M, Brechenmacher L, Cheng J, Xu D, Stacey G (2010) Root hair systems biology. Trends Plant Sci 15:641鈥?50PubMed View Article
  Marc J, Granger CL, Brincat J, Fisher DD, Kao T, McCubbin AG, Cyr RJ (1998) A GFP鈥揗AP4 reporter gene for visualizing cortical microtubule rearrangements in living epidermal cells. Plant Cell 10:1927鈥?939PubMed Central PubMed
  Miller DD, De Ruijter NCA, Emons AMC (1997) From signal to form: aspects of the cytoskeleton-plasma membrane-cell wall continuum in root hair tips. J Exp Bot 48:1881鈥?896
  Miller DD, De Ruijter NCA, Bisseling T (1999) The role of actin in root hair morphogenesis: studies with lipochito-oligosaccharide as a growth stimulator and cytochalasin as an actin perturbing drug. Plant J 17:141鈥?54View Article
  Ove膷ka M, Lang I, Balu拧ka F, Ismail A, Ille拧 P, Lichtscheidl IK (2005) Endocytosis and vesicle trafficking during tip growth of root hairs. Protoplasma 226:39鈥?4PubMed View Article
  Pei W, Du F, Zhang Y, He T, Ren H (2012) Control of the actin cytoskeleton in root hair development. Plant Sci 187:10鈥?8PubMed View Article
  Sliwinska E, Mathur J, Bewley JD (2012) Synchronously developing collet hairs in Arabidopsis thaliana provide an easily accessible system for studying nuclear movement and endoreduplication. J Exp Bot 63:4165鈥?178PubMed View Article
  Staiger CJ (2000) Signaling to the actin cytoskeleton in plants. Annu Rev Plant Physiol Plant Mol Biol 51:257鈥?88PubMed View Article
  Staiger CJ, Sheahan MB, Khurana P, Wang X, McCurdy DW, Blanchoin L (2009) Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array. J Cell Biol 184:269鈥?80PubMed Central PubMed View Article
  Starr DA (2007) Communication between the cytoskeleton and the nuclear envelope to position the nucleus. Mol Bio Syst 3:583鈥?89
  Starr DA, Han M (2002) Role of ANC-1 in tethering nuclei to the actin cytoskeleton. Science 298:406鈥?09PubMed View Article
  Starr DA, Han M (2003) ANChors away: an actin based mechanism of nuclear positioning. J Cell Sci 116:211鈥?21PubMed View Article
  Tamura K, Iwabuchi K, Fukao Y, Kondo M, Okamoto K, Ueda H, Nishimura M, Hara-Nishimura I (2013) Myosin XI-i links the nuclear membrane to the cytoskeleton to control nuclear movement and shape in Arabidopsis. Curr Biol 23:1776鈥?781PubMed View Article
  Wang X, Zhu L, Liu B, Wang C, Jin L, Zhao Q, Yuan M (2007) Arabidopsis MICROTUBULE-ASSOCIATED PROTEIN18 functions in directional cell growth by destabilizing cortical microtubules. Plant Cell 19:877鈥?89PubMed Central PubMed View Article
  Wang YS, Yoo CM, Blancaflor EB (2008) Improved imaging of actin filaments in transgenic Arabidopsis plants expressing a green fluorescent protein fusion to the C-and N-termini of the fimbrin actin-binding domain 2. New Phytol 177:525鈥?36PubMed
  Yoo C, Wen J, Motes CM, Sparks JA, Blancaflor EB (2008) A class I ADP-ribosylation factor GTPase-activating protein is critical for maintaining directional root hair growth in Arabidopsis. Plant Physiol 147:1659鈥?674PubMed Central PubMed View Article
  Zhang Y, Xiao YY, Du F, Cao LJ, Dong HJ, Ren HY (2011) Arabidopsis VILLIN4 is involved in root hair growth through regulating actin organization in a Ca2+-dependent manner. New Phytol 190:667鈥?82PubMed View Article
  Zhu L, Zhang Y, Kang E, Xu Q, Wang M, Rui Y, Liu B, Yuan M, Fu Y (2013) MAP18 regulates the direction of pollen tube growth in Arabidopsis by modulating F-actin organization. Plant Cell 25:851鈥?67PubMed Central PubMed View Article
  
• 作者单位：Yan Zhang (1)
  Erfang Kang (1)
  Ming Yuan (1)
  Ying Fu (1)
  Lei Zhu (1)
  
  1. State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing, 100193, China
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Cell Biology
  Plant Sciences
  Biotechnology
  Plant Biochemistry
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-203X

文摘

Key message PCaP2 plays a key role in maintaining the nucleus at a relatively fixed distance from the apex during root hair growth by modulating actin filaments. Abstract During root hair growth, the nucleus localizes at a relatively fixed distance from the apex. In Arabidopsis thaliana, the position of the nucleus is mainly dependent on the configuration of microfilaments (filamentous actin). However, the mechanisms underlying the regulation of actin dynamics and organization for nuclear positioning are largely unknown. In the present study, we demonstrated that plasma membrane-associated Ca2+ binding protein 2 (PCaP2) influences the position of the nucleus during root hair growth. Abnormal expression of PCaP2 in pcap2 and PCaP2 over-expression plants led to the disorganization of actin filaments, rather than microtubules, in the apex and sub-apical regions of root hairs, which resulted in aberrant root hair growth patterns and misplaced nuclei. Analyses using a PCaP2 mutant protein revealed that actin-severing activity is essential for the function of PCaP2 in root hairs. We demonstrated that PCaP2 plays a key role in maintaining nuclear position in growing root hairs by modulating actin filaments.